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J Neurosci. 2014 Jul 23;34(30):9927-44. doi: 10.1523/JNEUROSCI.4567-13.2014.

Neuronal ensemble synchrony during human focal seizures.

Author information

1
Department of Neuroscience, Institute for Brain Science and Center for Neurorestoration and Neurotechnology, Department of Veterans Affairs, Providence, Rhode Island 02912, wilson_truccolo@brown.edu.
2
Department of Neurology.
3
Division of Applied Mathematics, Brown University, Providence, Rhode Island 02912.
4
Department of Neurosurgery, and Nayef Al-Rodhan Laboratories for Cellular Neurosurgery and Neurosurgical Technology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114.
5
Department of Neurosurgery, Alpert Medical School, Brown University, Providence, Rhode Island 02912, Norman Prince Neurosciences Institute, Brown University, Providence, Rhode Island 02912.
6
Department of Neurosurgery, Children's Hospital and Harvard Medical School, Boston, Massachusetts 02114, and Department of Neurosurgery and.
7
Department of Neurology and.
8
School of Engineering, and Institute for Brain Science and Center for Neurorestoration and Neurotechnology, Department of Veterans Affairs, Providence, Rhode Island 02912, Department of Neurology, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02114.

Abstract

Seizures are classically characterized as the expression of hypersynchronous neural activity, yet the true degree of synchrony in neuronal spiking (action potentials) during human seizures remains a fundamental question. We quantified the temporal precision of spike synchrony in ensembles of neocortical neurons during seizures in people with pharmacologically intractable epilepsy. Two seizure types were analyzed: those characterized by sustained gamma (∼40-60 Hz) local field potential (LFP) oscillations or by spike-wave complexes (SWCs; ∼3 Hz). Fine (<10 ms) temporal synchrony was rarely present during gamma-band seizures, where neuronal spiking remained highly irregular and asynchronous. In SWC seizures, phase locking of neuronal spiking to the SWC spike phase induced synchrony at a coarse 50-100 ms level. In addition, transient fine synchrony occurred primarily during the initial ∼20 ms period of the SWC spike phase and varied across subjects and seizures. Sporadic coherence events between neuronal population spike counts and LFPs were observed during SWC seizures in high (∼80 Hz) gamma-band and during high-frequency oscillations (∼130 Hz). Maximum entropy models of the joint neuronal spiking probability, constrained only on single neurons' nonstationary coarse spiking rates and local network activation, explained most of the fine synchrony in both seizure types. Our findings indicate that fine neuronal ensemble synchrony occurs mostly during SWC, not gamma-band, seizures, and primarily during the initial phase of SWC spikes. Furthermore, these fine synchrony events result mostly from transient increases in overall neuronal network spiking rates, rather than changes in precise spiking correlations between specific pairs of neurons.

KEYWORDS:

collective dynamics; conditional inference; epilepsy; maximum entropy

PMID:
25057195
PMCID:
PMC4107409
DOI:
10.1523/JNEUROSCI.4567-13.2014
[Indexed for MEDLINE]
Free PMC Article

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